CDK1 inhibition targets the p53-NOXA-MCL1 axis, selectively kills embryonic stem cells, and prevents teratoma formation

Stem Cell Reports

Volumn 4, Issue 3, 2015, Pages 374-389

  Huskey, Noelle E ^a   Guo, Tingxia ^a   Evason, Kimberley J ^a,b   Momcilovic, Olga ^a   Pardo, David ^a   Creasman, Katelyn J ^a   Judson, Robert L ^a   Blelloch, Robert ^a   Oakes, Scott A ^b,c   Hebrok, Matthias ^a   Goga, Andrei ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN A; CYCLIN B1; CYCLIN B2; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE INHIBITOR 1; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN BCL 2; PROTEIN MCL 1; PROTEIN NOXA; PROTEIN P53; MCL1 PROTEIN, MOUSE; PMAIP1 PROTEIN, MOUSE; PROTEIN KINASE INHIBITOR;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CELL PROLIFERATION; CELL SURVIVAL; DNA CONTENT; DNA DAMAGE; EMBRYONIC STEM CELL; ENZYME INHIBITION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUCLEAR EXPORT SIGNAL; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; TERATOMA; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL DIFFERENTIATION; CELL LINE; CELL TRANSFORMATION; CYTOLOGY; DRUG EFFECTS; DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETICS; METABOLISM; PATHOLOGY; RNA INTERFERENCE;

ANIMALS; APOPTOSIS; CDC2 PROTEIN KINASE; CELL DIFFERENTIATION; CELL LINE; CELL TRANSFORMATION, NEOPLASTIC; CYCLIN A; CYCLIN B1; CYCLIN B2; DNA DAMAGE; DRUG RESISTANCE; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION; GENE KNOCKOUT TECHNIQUES; HUMANS; MICE; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; OCTAMER TRANSCRIPTION FACTOR-3; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-BCL-2; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TERATOMA; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84924541933     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2015.01.019     Document Type: Article

References (45)

1. A. Ballabeni, I.H. Park, R. Zhao, W. Wang, P.H. Lerou, G.Q. Daley, and M.W. Kirschner Cell cycle adaptations of embryonic stem cells Proc. Natl. Acad. Sci. USA 108 2011 19252 19257
2. C. Barrière, D. Santamaría, A. Cerqueira, J. Galán, A. Martín, S. Ortega, M. Malumbres, P. Dubus, and M. Barbacid Mice thrive without Cdk4 and Cdk2 Mol. Oncol. 1 2007 72 83
3. K.A. Becker, P.N. Ghule, J.A. Therrien, J.B. Lian, J.L. Stein, A.J. van Wijnen, and G.S. Stein Self-renewal of human embryonic stem cells is supported by a shortened G1 cell cycle phase J. Cell. Physiol. 209 2006 883 893
4. E.E. Brooks, N.S. Gray, A. Joly, S.S. Kerwar, R. Lum, R.L. Mackman, T.C. Norman, J. Rosete, M. Rowe, and S.R. Schow CVT-313, a specific and potent inhibitor of CDK2 that prevents neointimal proliferation J. Biol. Chem. 272 1997 29207 29211
5. C.E. Canman, D.S. Lim, K.A. Cimprich, Y. Taya, K. Tamai, K. Sakaguchi, E. Appella, M.B. Kastan, and J.D. Siliciano Activation of the ATM kinase by ionizing radiation and phosphorylation of p53 Science 281 1998 1677 1679
6. L. Chen, S.N. Willis, A. Wei, B.J. Smith, J.I. Fletcher, M.G. Hinds, P.M. Colman, C.L. Day, J.M. Adams, and D.C. Huang Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function Mol. Cell 17 2005 393 403
7. J. Deng, N. Carlson, K. Takeyama, P. Dal Cin, M. Shipp, and A. Letai BH3 profiling identifies three distinct classes of apoptotic blocks to predict response to ABT-737 and conventional chemotherapeutic agents Cancer Cell 12 2007 171 185
8. M.A. Dickson, and G.K. Schwartz Development of cell-cycle inhibitors for cancer therapy Curr. Oncol. 16 2009 36 43
9. J. Falck, J.V. Forment, J. Coates, M. Mistrik, J. Lukas, J. Bartek, and S.P. Jackson CDK targeting of NBS1 promotes DNA-end resection, replication restart and homologous recombination EMBO Rep. 13 2012 561 568
10. A. Goga, D. Yang, A.D. Tward, D.O. Morgan, and J.M. Bishop Inhibition of CDK1 as a potential therapy for tumors over-expressing MYC Nat. Med. 13 2007 820 827
11. N.S. Gray, L. Wodicka, A.M. Thunnissen, T.C. Norman, S. Kwon, F.H. Espinoza, D.O. Morgan, G. Barnes, S. LeClerc, and L. Meijer Exploiting chemical libraries, structure, and genomics in the search for kinase inhibitors Science 281 1998 533 538
12. T. Guo, L. Landsman, N. Li, and M. Hebrok Factors expressed by murine embryonic pancreatic mesenchyme enhance generation of insulin-producing cells from hESCs Diabetes 62 2013 1581 1592
13. P. Hauck, B.H. Chao, J. Litz, and G.W. Krystal Alterations in the Noxa/Mcl-1 axis determine sensitivity of small cell lung cancer to the BH3 mimetic ABT-737 Mol. Cancer Ther. 8 2009 883 892
14. D. Horiuchi, N.E. Huskey, L. Kusdra, L. Wohlbold, K.A. Merrick, C. Zhang, K.J. Creasman, K.M. Shokat, R.P. Fisher, and A. Goga Chemical-genetic analysis of cyclin dependent kinase 2 function reveals an important role in cellular transformation by multiple oncogenic pathways Proc. Natl. Acad. Sci. USA 109 2012 E1019 E1027
15. N. Johnson, Y.C. Li, Z.E. Walton, K.A. Cheng, D. Li, S.J. Rodig, L.A. Moreau, C. Unitt, R.T. Bronson, and H.D. Thomas Compromised CDK1 activity sensitizes BRCA-proficient cancers to PARP inhibition Nat. Med. 17 2011 875 882
16. I. Kalaszczynska, Y. Geng, T. Iino, S. Mizuno, Y. Choi, I. Kondratiuk, D.P. Silver, D.J. Wolgemuth, K. Akashi, and P. Sicinski Cyclin A is redundant in fibroblasts but essential in hematopoietic and embryonic stem cells Cell 138 2009 352 365
17. S. Keeney, and M.J. Neale Initiation of meiotic recombination by formation of DNA double-strand breaks: mechanism and regulation Biochem. Soc. Trans. 34 2006 523 525
18. S. Kobayashi, S.H. Lee, X.W. Meng, J.L. Mott, S.F. Bronk, N.W. Werneburg, R.W. Craig, S.H. Kaufmann, and G.J. Gores Serine 64 phosphorylation enhances the antiapoptotic function of Mcl-1 J. Biol. Chem. 282 2007 18407 18417
19. V.C. Li, A. Ballabeni, and M.W. Kirschner Gap 1 phase length and mouse embryonic stem cell self-renewal Proc. Natl. Acad. Sci. USA 109 2012 12550 12555
20. J.C. Liu, X. Guan, J.A. Ryan, A.G. Rivera, C. Mock, V. Agrawal, A. Letai, P.H. Lerou, and G. Lahav High mitochondrial priming sensitizes hESCs to DNA-damage-induced apoptosis Cell Stem Cell 13 2013 483 491 Erratum in Cell Stem Cell. 2013;13:634. Agarwal, Vishesh [corrected to Agrawal, Vishesh]
21. S.J. Micallef, X. Li, J.V. Schiesser, C.E. Hirst, Q.C. Yu, S.M. Lim, M.C. Nostro, D.A. Elliott, F. Sarangi, and L.C. Harrison INS(GFP/w) human embryonic stem cells facilitate isolation of in vitro derived insulin-producing cells Diabetologia 55 2012 694 706
22. O. Momcilovic, L. Knobloch, J. Fornsaglio, S. Varum, C. Easley, and G. Schatten DNA damage responses in human induced pluripotent stem cells and embryonic stem cells PLoS ONE 5 2010 e13410
23. D.O. Morgan The Cell Cycle: Principles of Control 2007 New Science Press
24. W. Nakajima, M.A. Hicks, N. Tanaka, G.W. Krystal, and H. Harada Noxa determines localization and stability of MCL-1 and consequently ABT-737 sensitivity in small cell lung cancer Cell Death Dis. 5 2014 e1052
25. I. Neganova, X. Zhang, S. Atkinson, and M. Lako Expression and functional analysis of G1 to S regulatory components reveals an important role for CDK2 in cell cycle regulation in human embryonic stem cells Oncogene 28 2009 20 30
26. K.W. Orford, and D.T. Scadden Deconstructing stem cell self-renewal: genetic insights into cell-cycle regulation Nat. Rev. Genet. 9 2008 115 128
27. D. Parry, T. Guzi, F. Shanahan, N. Davis, D. Prabhavalkar, D. Wiswell, W. Seghezzi, K. Paruch, M.P. Dwyer, and R. Doll Dinaciclib (SCH 727965), a novel and potent cyclin-dependent kinase inhibitor Mol. Cancer Ther. 9 2010 2344 2353
28. S.E. Peterson, Y. Li, B.T. Chait, M.E. Gottesman, R. Baer, and J. Gautier Cdk1 uncouples CtIP-dependent resection and Rad51 filament formation during M-phase double-strand break repair J. Cell Biol. 194 2011 705 720
29. C. Ploner, R. Kofler, and A. Villunger Noxa: at the tip of the balance between life and death Oncogene 27 Suppl 1 2008 S84 S92
30. K. Sabapathy, M. Klemm, R. Jaenisch, and E.F. Wagner Regulation of ES cell differentiation by functional and conformational modulation of p53 EMBO J. 16 1997 6217 6229
31. D. Santamaría, C. Barrière, A. Cerqueira, S. Hunt, C. Tardy, K. Newton, J.F. Cáceres, P. Dubus, M. Malumbres, and M. Barbacid Cdk1 is sufficient to drive the mammalian cell cycle Nature 448 2007 811 815
32. A. Schnerch, C. Cerdan, and M. Bhatia Distinguishing between mouse and human pluripotent stem cell regulation: the best laid plans of mice and men Stem Cells 28 2010 419 430
33. T.C. Schulz, H.Y. Young, A.D. Agulnick, M.J. Babin, E.E. Baetge, A.G. Bang, A. Bhoumik, I. Cepa, R.M. Cesario, and C. Haakmeester A scalable system for production of functional pancreatic progenitors from human embryonic stem cells PLoS ONE 7 2012 e37004
34. Y. Shiloh ATM and related protein kinases: safeguarding genome integrity Nat. Rev. Cancer 3 2003 155 168
35. E. Stead, J. White, R. Faast, S. Conn, S. Goldstone, J. Rathjen, U. Dhingra, P. Rathjen, D. Walker, and S. Dalton Pluripotent cell division cycles are driven by ectopic Cdk2, cyclin A/E and E2F activities Oncogene 21 2002 8320 8333
36. K. Takahashi, and S. Yamanaka Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors Cell 126 2006 663 676
37. O. Takeuchi, J. Fisher, H. Suh, H. Harada, B.A. Malynn, and S.J. Korsmeyer Essential role of BAX,BAK in B cell homeostasis and prevention of autoimmune disease Proc. Natl. Acad. Sci. USA 102 2005 11272 11277
38. O. Tetsu, and F. McCormick Proliferation of cancer cells despite CDK2 inhibition Cancer Cell 3 2003 233 245
39. Z. Ullah, M.J. Kohn, R. Yagi, L.T. Vassilev, and M.L. DePamphilis Differentiation of trophoblast stem cells into giant cells is triggered by p57/Kip2 inhibition of CDK1 activity Genes Dev. 22 2008 3024 3036
40. S. van den Heuvel, and E. Harlow Distinct roles for cyclin-dependent kinases in cell cycle control Science 262 1993 2050 2054
41. L.T. Vassilev, C. Tovar, S. Chen, D. Knezevic, X. Zhao, H. Sun, D.C. Heimbrook, and L. Chen Selective small-molecule inhibitor reveals critical mitotic functions of human CDK1 Proc. Natl. Acad. Sci. USA 103 2006 10660 10665
42. K.H. Vousden, and X. Lu Live or let die: the cell's response to p53 Nat. Rev. Cancer 2 2002 594 604
43. Y. Wang, R. Medvid, C. Melton, R. Jaenisch, and R. Blelloch DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell self-renewal Nat. Genet. 39 2007 380 385
44. M.C. Wei, W.X. Zong, E.H. Cheng, T. Lindsten, V. Panoutsakopoulou, A.J. Ross, K.A. Roth, G.R. MacGregor, C.B. Thompson, and S.J. Korsmeyer Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death Science 292 2001 727 730
45. Y. Zhang, and Y. Xiong A p53 amino-terminal nuclear export signal inhibited by DNA damage-induced phosphorylation Science 292 2001 1910 1915